Myctophid Feeding Ecology and Carbon Transport along the ...
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Myctophid Feeding Ecology and Carbon Transport along the Northern Mid-Atlantic
Ridge
________________
A Thesis
Presented to
The Faculty of the School of Marine Science
The College of William and Mary in Virginia
In Partial Fulfillment
of the Requirements for the Degree of
Master of Science
________________
by
Jeanna M. Hudson
2012
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APPROVAL SHEET
This thesis is submitted in partial fulfillment of
the requirements for the degree of
Master of Science
_________________________________ Jeanna M. Hudson
Approved by the Committee October 22, 2012
_________________________________ John E. Graves, Ph.D.
Committee Co-Chairman/Co-Advisor
_________________________________ Deborah K. Steinberg, Ph.D.
Committee Co-Chairman/Co-Advisor
_________________________________ Robert J. Diaz, Ph.D.
_________________________________ Robert J. Latour, Ph.D.
_________________________________ Michael Vecchione, Ph.D.
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TABLE OF CONTENTS
ACKNOWLEDGMENTS ................................................................................................. iv
LIST OF TABLES ...............................................................................................................v
LIST OF FIGURES ........................................................................................................... vi
ABSTRACT ...................................................................................................................... vii
INTRODUCTION ...............................................................................................................2 Myctophid ecology and potential role in carbon export ..........................................2 The Mid-Atlantic Ridge and the MAR-ECO study .................................................5 Pelagic fish community structure of the Mid-Atlantic Ridge ..................................7 Objectives and significance of the study .................................................................9
METHODS ........................................................................................................................12 Sampling procedure ...............................................................................................12 Myctophid selection, dissection, and prey identification .......................................12 Prey measurements ................................................................................................14 General diet description .........................................................................................14 Ontogenetic and spatial changes in diet .................................................................16 Gastric evacuation and daily consumption ............................................................17 Active carbon export by diel vertical migration ....................................................17
RESULTS ..........................................................................................................................19 General diet description .........................................................................................19 Ontogenetic and spatial changes in diet .................................................................20 Species interaction and the effect on spatial changes in diet .................................23 Gastric evacuation and daily consumption ............................................................24 Active carbon export by diel vertical migration ....................................................25
DISCUSSION ....................................................................................................................27
General diet description .........................................................................................27 Ontogenetic and spatial changes in diet .................................................................31 Daily consumption .................................................................................................37 Active carbon export by diel vertical migration ....................................................40
CONCLUSION ..................................................................................................................44
LITERATURE CITED ......................................................................................................46
VITA ..................................................................................................................................74
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ACKNOWLEDGMENTS
I am very grateful to Dr. Odd Aksel Bergstad and the members of the MAR-ECO program, without whom this work would not have been possible. I would like to especially thank Ingvar Byrkjedal for his assistance in deciphering museum specimen catalogs and for packaging and shipping myctophid samples. I am very appreciative to Dr. Tracey Sutton for providing me the opportunity to work with MAR-ECO and giving me my start in the field of deep-sea science.
I would like to thank my co-advisors, Dr. John Graves and Dr. Debbie Steinberg, for their support and willingness to help me succeed. John, thank you for the personal interest you took in my success and your constant encouragement. Your coaching for oral exams and record-breaking turn-around times for edits are truly appreciated. Debbie, thank you for pushing me to expand my thesis into the world of carbon. I truly feel it has positively contributed to my thesis and to the area of study. Your enthusiasm is infectious and could bring a smile to my face no matter how many hours I had spent on the microscope. Many thanks to Dr. Rob Latour for the countless hours of statistical guidance and his unwavering patience with me as I tried to keep up. I am so appreciative of your dedication to this project. To my remaining committee members, Dr. Mike Vecchione and Dr. Bob Diaz, thank you for your invaluable insight, comments, and discussions. I am very appreciative to Dr. Kam Tang for allowing me to use his lab space and equipment. Thank you to Dr. Linda Schaffner and the Office of the Associate Dean of Academic Studies for your support, in more ways than one. I am so thankful for everything you all have done for me. They say it takes a village to raise a child, and I am now certain that it also takes a village to complete a master’s thesis. There are so many fellow students who have helped me along the way and to whom I am very thankful. I was lucky enough to belong to two labs and have double the support and friendship of my lab mates. Thank you all for everything from presentation critiques and job advice, to lab dinners and canning adventures. Kristene Parsons and CJ Sweetman, you both have been such a source of support during my time at VIMS, and I am so lucky to be able to call you friends. A big thank you to Catarina Wor, Andre Buchheister, and Patrick Lynch for their invaluable statistical and R coding knowledge. And to the rest of my friends, we all helped to keep each other sane during this period of our lives, and I am thankful to have met every one of you! Finally, I owe, perhaps, the most thanks to my mother, Carol Miller, who always knew what I was capable of and refused to settle for less. Thank you for the love and the sacrifices it took to get me to where I am today. Thank you to my Grandpa, Joseph Voss, for all of his interest in my project and for the motivation to keep putting one fish in front of the other so that I could, at last, tell him, “Yes, I am finally finished with my fish!”. To the rest of my family, thank you for your support throughout this journey. And finally, my husband, Wes Hudson, I could not have done this without you by my side. You have helped me in so many ways and I am forever grateful for your unconditional love.
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LIST OF TABLES
Table Page 1. Diet composition of Benthosema glaciale, Protomyctophum arcticum, and Hygophum hygomii ......................................................................................................................... 55-57 2. Daily consumption and gut evacuation rates of Benthosema glaciale, Protomyctophum arcticum, and Hygophum hygomii .........................................................58 3. Active carbon transport by diel vertically migrating myctophids from the Mid-Atlantic Ridge ..................................................................................................................................59 4. Proportion of prey in diets of Benthosema glaciale and Protomyctophum arcticum caught simultaneously ........................................................................................................60
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LIST OF FIGURES
Figure Page 1. Trawl sampling stations along the northern Mid-Atlantic Ridge during leg 1 of the R/V G.O. Sars MAR-ECO expedition ..............................................................................61 2. Standard length distribution of Benthosema glaciale, Protomyctophum arcticum, and Hygophum hygomii ............................................................................................................62 3. Cluster diagram (A) and scree plot (B) for Benthosema glaciale ...............................64 4. Canonical correspondence analysis biplot for Benthosema glaciale ..........................66 5. Diet composition of Benthosema glaciale by ridge section (A) and time of day (B) ................................................................................................................................ 68-69 6. Canonical correspondence analysis biplot for Protomyctophum arcticum .................70 7. Diet composition of Protomyctophum arcticum by depth zone ..................................71 8. Canonical correspondence analysis of Benthosema glaciale and Protomyctophum
arcticum including all samples (A) and only samples collected simultaneously (B) ..73
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ABSTRACT
The Mid-Atlantic Ridge (MAR) is the largest topographic feature in the Atlantic
Ocean, yet little is known about the food web structure and trophic ecology of fishes
inhabiting mesopelagic waters along the MAR. To better understand the food web
structure and to compare the feeding ecology of abundant MAR fishes to those in off-
ridge areas, MAR-ECO, a Mid-Atlantic Ridge ecosystem field project of the Census of
Marine Life, sampled the pelagic fauna of the northern MAR (Iceland to the Azores)
during June-July, 2004. Samples were collected with two midwater trawls outfitted with
multiple opening and closing cod ends to sample discrete depths from the surface to
>2300 m at predefined stations within four ridge sections. Fishes of the family
Myctophidae were the most abundant fishes collected, with the myctophid Benthosema
glaciale the numerically dominant species. The feeding ecology of three myctophid
species, B. glaciale, Protomyctophum arcticum, and Hygophum hygomii, were quantified
through dietary analysis. Each species was predominantly zooplanktivorous, consuming
copepods, euphausiids, ostracods, and other crustacean zooplankton, with each
myctophid species exhibiting unique dietary patterns. Different abiotic parameters
influenced variability in the diet of B. glaciale and P. arcticum as determined by
canonical correspondence analysis. Of the measured parameters, ridge section and time
of day were significant explanatory variables in the diet of B. glaciale, while only depth
was significant in the diet of P. arcticum. Daily consumption by B. glaciale and P.
arcticum was highest at the Reykjanes Ridge and Charlie-Gibbs Fracture Zone,
respectively; consumption by H. hygomii was only measured at the Azorean Zone. Daily
consumption of all three species was less than 1% of dry body weight. Active transport
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of carbon out of the euphotic zone by diel vertically migrating MAR myctophids through
respiration of CO2, excretion of dissolved organic carbon, and egestion of particulate
organic carbon (POC) was also estimated, and compared to passive sinking of POC in the
North Atlantic. Active carbon flux by the 0-200 m integrated migrant myctophid
biomass, uncorrected for trawl efficiency, ranged from 0.01-0.4% of sinking POC flux at
150 m and 0.02-0.95% at 300 m. If myctophid biomass was corrected for low gear
efficiency, flux increased to 0.1-1% and 0.3-3.5%, respectively, of sinking POC. Lower
MAR myctophid biomass resulted in lower active carbon transport compared to
myctophids in the Pacific and zooplankton in the North Atlantic estimated in previous
studies, but myctophid active transport should still be considered in models of MAR
carbon cycling. Due to the role of myctophids as both predators of numerous
zooplankton taxa and as prey of higher taxa, information on the feeding ecology and
daily consumption of these fishes is necessary to accurately assess their role in the MAR
food web and the overall trophic structure of this hydrodynamically and topographically
unique ecosystem.
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Myctophid Feeding Ecology and Carbon Transport along the Northern Mid-Atlantic
Ridge
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INTRODUCTION
Fishes of the family Myctophidae are an integral part of the trophodynamics of
oceanic ecosystems around the world, including the North Atlantic Ocean. The diets of
myctophids are probably most well known from the eastern and western sides of the
North Atlantic Ocean; however, the feeding ecology and role in carbon cycling of
myctophids associated with the northern Mid-Atlantic Ridge (MAR), part of the largest
topographic feature in the Atlantic Ocean, is completely unknown. The purpose of this
thesis is to compare the feeding ecology of, and carbon export by, myctophids at the
MAR to myctophids in off-ridge areas of the North Atlantic and other ocean basins.
Myctophid ecology and potential role in carbon export
Fishes of the family Myctophidae are distributed globally and reside from the
surface to depths greater than 1000 m. They are the most numerically abundant
mesopelagic fish family in many areas around the world (Frost and McCrone 1979,
Balanov and Il’inskii 1992, Beamish et al. 1999, Sutton et al. 2008). Information on the
feeding ecology and trophic position of these fishes is critical to the understanding of
ecosystem food webs and modeling of large-scale ecological processes in the ocean.
Myctophids generally occupy a tertiary trophic level, feeding primarily on
crustacean zooplankton, but they are also known to feed on gelatinous zooplankton,
pteropods, and other non-crustacean prey including other fishes (Kinzer 1982, Sameoto
1988, Hopkins et al. 1996, Moku et al. 2000). Hopkins et al. (1996) found that
myctophids were the most important consumer in a Gulf of Mexico assemblage
consisting of 164 species representing 16 families of midwater fishes, ingesting 31% of
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the total prey biomass consumed daily by the assemblage. In the eastern Gulf of Mexico,
a low-latitude myctophid community consumed 8-16% of the total copepod daily
production and 2% of the overall zooplankton biomass each night (Hopkins and Gartner
1992). Gorelova (1984) estimated that myctophids may consume 2-31% (average 10%)
of the zooplankton standing stock daily in the equatorial Pacific. A wide range of daily
consumption has been estimated for myctophids, generally falling within 1-6% of body
weight for adults (Sameoto 1988, Pahkomov et al. 1996, Brodeur and Yamamura 2005).
While myctophids are important predators, they are also important prey for higher
order predators such as marine mammals, sea birds, and piscivorous fishes (Hopkins et al.
1996, Beamish et al. 1999, Pusineri et al. 2008, Pereira et al. 2011). The diet of stomiid
fishes in a Gulf of Mexico assemblage was comprised mainly of fishes (83% of
abundance), of which myctophids represented 42% (Hopkins et al. 1996). Myctophids
have also been identified in the diets of swordfish, albacore tuna, common dolphin,
striped dolphin and beaked whales, constituting as much as 50% of the diet by mass
(Pusineri et al. 2008, Pereira et al. 2011). Beamish et al. (1999) postulated that
myctophids may constitute up to 90% of the diets of northern fur seal, Dall’s Porpoise,
Pacific white-sided dolphin, and northern right whale dolphin in the subarctic Pacific.
Additionally, myctophids were a notable component of the diet of many sea birds in this
area, including several species of puffins, murres, and kittiwakes (Beamish et al. 1999).
Many myctophid species make daily vertical migrations up to the epipelagic zone
at night to feed on zooplankton, and migrate to deeper water (~300-1000 m) during the
day where they digest their food. While metabolizing this surface-derived food at depth,
myctophids egest large, fast-sinking, carbon-rich fecal pellets, respire carbon dioxide, and
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excrete dissolved organic carbon and dissolved organic and inorganic nitrogen. This
“active transport” of organic and inorganic nutrients may be an important component of
the biological pump (collectively the vertical export of surface-derived nutrients to depth
by vertically migrating zooplankton and fishes, ‘passive’ sinking of dead phytoplankton
aggregates and of fecal pellets, and physical mixing of dissolved organic matter) and
subsidizes the metabolic demands of deep-sea organisms in an extremely food-limited
environment (Vinogradov 1962, Steinberg et al. 2000, 2008, Hidaka et al. 2001, Wotton
and Malmqvist 2001). Hidaka et al. (2001) found the respiratory flux due to vertically
migrating micronekton in the western equatorial Pacific (biomass corrected for assumed
gear sampling efficiency of 14%) to be between 15-30 mg C m-2 d-1, which accounted for
28-55% of the sinking particulate organic carbon (POC) flux, while the gut flux (material
consumed near the surface that is egested as fecal pellets at depth) accounted for 2-3% of
POC flux. Respiratory and gut fluxes due to migrant myctophids accounted for
approximately 14-26% and 1-2%, respectively, of the POC flux. In addition, Wilson et
al. (2009) reported that carbonate production within the intestines of marine fishes, which
is released via excretion, contributes 3-15% of total oceanic carbonate production. Given
that myctophids are the dominant group of vertically migrating fishes and account for the
greatest proportion of fish biomass in the epipelagic zone at night (Maynard et al. 1975,
Hopkins and Lancraft 1984), myctophids have the potential to export a significant
amount of organic and inorganic carbon to the deep sea.
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The Mid-Atlantic Ridge and the MAR-ECO study
The continental slope regions of the ocean make up a small proportion of the
earth’s surface area (Garrison 2010). Beyond the narrow continental slope, organisms in
the mesopelagic zone rarely encounter land. The high pressures and cold temperatures
prevent most mesopelagic organisms from reaching the sea floor, except at seamounts
and mid-ocean ridges. Mid-ocean ridges, abrupt, hard-bottomed topographic features
that stretch 65,000 km around the world (Garrison 2010), protrude up into the water
column to create relatively shallow, diverse habitat structure in an otherwise structurally
homogeneous medium. In the Atlantic Ocean the Mid-Atlantic Ridge (MAR) divides the
ocean into nearly equal eastern and western halves. It provides a unique, relatively
shallow habitat in the center of the deep Atlantic Ocean and supports a diverse faunal
assemblage (Vecchione et al. 2010). The MAR exhibits many unique topographical
features including the Charlie-Gibbs Fracture Zone, where deep sub-marine rift valleys
run east to west and influence local and regional circulation patterns. Such alterations in
circulation patterns may affect the distribution and feeding ecology of deep-sea
organisms including those that inhabit the ridge as well as transient (migratory) species
(Roden 1987, Bergstad and Godø 2003, Sutton et al. 2008). To date, few ecological
studies have focused on the ridge, and hence, little is known about the fauna and ecology
of MAR communities.
In 2001, the Census of Marine Life, a 10-year international effort to assess the
diversity, distribution, and abundance of marine life, enacted a field project titled
Patterns and Processes of the Ecosystem of the Northern Mid-Atlantic (MAR-ECO).
This project aimed to describe and understand the patterns of distribution, abundance, and
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trophic relationships of organisms inhabiting and associated with the northern MAR
between Iceland and the Azores (Bergstad 2002). Describing the ecological processes
that cause variability in these patterns is fundamental to understanding the influence of
the MAR on this dynamic ecosystem.
One goal of MAR-ECO was to determine if the trophic structure of the northern
MAR ecosystem is similar to that of continental slope regions of the eastern and western
Atlantic. The presence of the MAR in the bathypelagic realm, and to a lesser extent in
the mesopelagic realm, provides the potential for unique faunal interactions and nutrient
availability. Elevated levels of primary productivity and chlorophyll, which are often
associated with seamounts, mid-ocean ridges, and frontal zones in oligotrophic regions
(Genin and Boehlert 1985, Dower et al. 1992, Muriño et al. 2001), have the potential to
support enhanced secondary production and higher order epi- and mesopelagic biomass.
Benthopelagic organisms associated with the ridge surface are supported through
resuspension of sediment and through predation on pelagic fauna. Non-migrating pelagic
fauna become susceptible to predation through advection to the ridge by water currents,
while vertically migrating mesopelagic fauna become trapped by the elevated seafloor
during their daily migratory descent (Genin and Dower 2007, Porteiro and Sutton 2007).
Due to the potential for enhanced nutrient availability and faunal interactions at the
MAR, this ecosystem may support a unique community and trophic structure compared
to off-ridge waters.
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Pelagic fish community structure of the Mid-Atlantic Ridge
To investigate the diversity, community structure, and trophic ecology of
organisms inhabiting the MAR, MAR-ECO sampled the epi-, meso-, and bathypelagic
fauna during a two-part expedition to the ridge during June-July, 2004 aboard the
Norwegian vessel R/V G.O. Sars. These cruises were two of many MAR-ECO sampling
expeditions to the MAR with the goal of assessing the occurrence, distribution, and
ecology of animals and animal communities along the ridge between Iceland and the
Azores (Figure 1). Leg 1 of this expedition sampled the pelagic fauna and is the focus of
my thesis.
Sampling during leg 1 resulted in the collection of 205 fish species and the
classification of the faunal composition within four sections along the MAR and five
depth zones (see Methods for description of depth zones). A detailed description of the
community structure of the MAR is provided by Sutton et al. (2008). The MAR
ecosystem is unique in many ways compared to the surrounding areas of the eastern and
western Atlantic. A decrease in faunal abundance and biomass with increasing depth is
typically expected for open ocean ecosystems; however, the pelagic MAR fauna
exhibited higher than expected abundance and biomass at bathypelagic depths (Sutton et
al. 2008). Depth distributions of some MAR fishes were unique in that many species
were found over the ridge at depths deeper and shallower than previously recorded, and
demersal fish biomass was highest at stations near the summit of the ridge (Bergstad et al.
2008). Community composition of mesopelagic fishes along the ridge was fairly
consistent north of the Sub-polar Front, a prominent hydrologic feature crossing the
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MAR between 45-52°N, which appeared to act as a boundary to the northward
distribution of many southern species.
Fishes of the families Myctophidae, Gonostomatidae, Microstomatidae,
Stomiidae, and Melamphidae were abundant throughout the ridge with vertically
migrating myctophids dominating the 200-750 m depth zone. Forty-five myctophid
species were caught along the ridge, however only nine species comprised more than 1%
of the total myctophid abundance by number. In accordance with typical trends of
abundance and species richness at high latitudes, the fish assemblage in the three northern
ridge sections in the 200-750 m depth zone comprised only a few abundant species,
predominantly myctophids. There was a shift in community composition at the Azorean
Zone (AZ) ridge section within the same depth zone. Here, species richness was much
higher than farther north and the abundance of each species decreased.
The most abundant fish collected from the ridge during leg 1 of the MAR-ECO
cruise was the myctophid Benthosema glaciale. This species made up over half of the
abundance by number and one quarter of the biomass in the three northern ridge sections
from 0-750 m but only 6% and 4%, respectively, in the AZ (Sutton et al. 2008).
Benthosema glaciale was also very abundant in deeper waters up to 1500 m in the
Faraday Seamount Zone (FSZ) and AZ due to cooler waters occurring deeper at lower
latitudes. While B. glaciale exhibited a wide geographic distribution across all four ridge
sections, other species, such as Protomyctophum arcticum, appeared to be more limited
in their distribution. Protomyctophum arcticum was numerically abundant in the two
northern ridge sections with only a few individuals caught at the FSZ and was not
captured in the AZ. The distributions of several myctophid species were limited to a
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single ridge section, notably the AZ. In this ridge section, 29 myctophid species made up
half of the abundance in the 0-750 m depth zone and the myctophid Lobianchia dofleini
replaced B. glaciale as the numerically dominant species, making up 19% of the
abundance and 7% of the biomass (Sutton et al. 2008). The myctophid Hygophum
hygomii, was unique in that it was a moderately abundant species (2.7% by number)
found only at the AZ.
Much is known of the feeding ecology of B. glaciale in the North Atlantic;
however, active carbon transport by myctophids in this area has not been studied. Very
little information exists on the feeding ecology of other species, such as P. arcticum and
H. hygomii, despite their high abundance. Notwithstanding the ample diet data for some
North Atlantic myctophids, comprehensive feeding ecology of myctophids inhabiting the
MAR, the largest topographic feature in the Atlantic Ocean, is unknown. Being that
myctophids were the most abundant fishes collected from the MAR, and the importance
of these fishes as consumers of plankton and prey for many higher order predators,
information on the feeding ecology of and carbon transport by these fishes is necessary
for an accurate portrayal of food web structure and carbon cycling in the MAR
ecosystem.
Objectives and significance of the study
The main objective of this study was to describe and quantify the feeding ecology
of MAR myctophids. A secondary objective was to quantify the contribution of vertically
migrating myctophids through the active transport of carbon to the MAR biological
pump. The feeding ecology and trophic importance of many species of myctophids from
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around the world have been studied; however, neither the diets of myctophids inhabiting
the ecologically distinctive MAR ecosystem nor the potential for carbon transport by
vertically migrating MAR myctophids have been investigated. To accomplish the first
objective, the diets of three myctophid species– B. glaciale, P. arcticum, and H. hygomii
were investigated by quantifying the prey composition using weight, abundance, and
frequency of occurrence indices. To relate the dietary information to the energy
requirements and changes in diet with growth of each species, daily consumption was
calculated and ontogenetic dietary shifts were explored. Multivariate analyses were used
to determine how fish size and different environmental variables influence variance in the
diet. To accomplish the second objective, the amount of carbon transported via
respiration, excretion, and egestion to mesopelagic depths by vertically migrating MAR
myctophids was quantified. This allowed for an estimation of the extent to which MAR
myctophids contribute to active carbon transport in comparison to passive sinking of
POC, and provide the first estimate of myctophid active transport in the North Atlantic
Ocean.
The results from this study provide a comprehensive account of the diet of three
abundant mesopelagic species of myctophids from the northern Mid-Atlantic Ridge
during the months of June and July. This time of year in the North Atlantic represents an
active feeding period for mesopelagic fishes, corresponding with spring phytoplankton
blooms and subsequent zooplankton blooms. As a result of the high relative abundance
and biomass of myctophids at the MAR, they have the potential to impart heavy
predation pressure on zooplankton and to provide an important source of carbon export
out of the euphotic zone through metabolism of surface-consumed food at midwater
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depths. Estimates of active transport by mesopelagic fishes are limited, and do not exist
for the MAR. These data provide carbon transport estimates for the most abundant
vertically migrating, mesopelagic fish family along the MAR that can be used in
biogeochemical models that simulate and predict total carbon flux from the euphotic
zone. Additionally, due to their intermediate trophic position, information on the diet and
feeding ecology of myctophids from the ridge is essential to the successful construction
of a MAR ecosystem food web to achieve an understanding of the trophodynamics of the
geographically and hydrodynamically unique MAR ecosystem.
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METHODS
Sampling procedure
Myctophids were collected during the R/V G.O. Sars research expedition to the
Mid-Atlantic Ridge (Iceland to the Azores) during June-July, 2004. Two double-warp,
multi-cod end midwater trawls were used to sample the ridge fauna at discrete depth
zones. The macrozooplankton trawl has a 6 x 6 m2 mouth opening, 6 mm stretched mesh
throughout its length, and was equipped with five opening and closing cod ends. The
Åkra trawl has a 20-35 m vertical mouth opening, 110 m door-spread, graded mesh to 22
mm (stretched), and was equipped with three multiple opening and closing cod ends.
Predefined stations along the ridge were sampled discretely within five depth
categories: 0-200, 200-750, 750-1500, 1500-2300, and >2300 m in four ridge sections
(Figure 1). Average tow duration was 3:43 (hours: minutes) (maximum 6:52, minimum
0:59). Each net was open for an average of 0:53 (maximum 4:46, minimum 0:08).
Samples were classified as day (D), dusk (DN), night (N), or dawn (ND) with dusk and
dawn samples defined as the start time of the net being one hour before to one hour after
sunset and sunrise, respectively (Sutton et al. 2008). Once on board, specimens were
sorted and either frozen, or preserved in 10% buffered formalin. Preserved samples were
identified and transferred to 70% ethanol in the laboratory. For additional detail
concerning net sampling aboard the R/V G.O. Sars see Wenneck et al. (2008).
Myctophid selection, dissection, and prey identification
The three species included in this study, Benthosema glaciale, Protomyctophum
arcticum, and Hygophum hygomii were chosen because they fulfilled multiple criteria
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that were needed to obtain a representative sample of the myctophid assemblage in order
to investigate trophic ecology and carbon transport. Each species was abundant, occurred
primarily in the mesopelagic zone, and was known to conduct diel vertical migration.
Benthosema glaciale was very abundant at all of the four ridge sections and was captured
in many tows at different depths and times throughout the day. Protomyctophum
arcticum was caught in high numbers at the two northern ridge sections at several
different depth and time-of-day combinations. Hygophum hygomii was caught only at
the southern ridge section, and while the limited geographic distribution restricted the
number of possible combinations of depth and time of capture, their numbers still
allowed for an adequate description of the diet. The unique geographic distribution of
each species allowed for comparisons not only among species, but also across ridge
sections and varying environmental regimes.
A subset of specimens from the total catch of the three species was randomly
selected for measurement and dissection from as many geographic-location, depth, and
time-of-day combinations as were available. A total of 380 fish belonging to three
species was included in this study: 265 B. glaciale, 76 P. arcticum, and 39 H. hygomii.
The standard length of each fish was measured to the nearest 0.1 mm from the tip of the
snout to the posterior edge of the caudal peduncle. The stomach and intestines were
removed and contents were identified to the lowest possible taxonomic level using a
Nikon SMZ 1000 dissecting microscope. Diet descriptions and analyses include prey
from stomachs only. Intestinal prey were not included in the diet description due to the
tendency for advanced digestion and low taxonomic resolution. Prey types that were
observed infrequently were grouped with more common genus or family classifications
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to avoid small sample sizes. Diet indices were calculated for the lowest taxonomic level
of grouped prey types that provided adequate sample size (Table 1) as well as broad prey
categories at the subclass level (e.g., copepod).
Prey measurements
The length and width of each prey item was determined to the nearest 0.01 mm
using Image Pro Plus 5.0 software. Cephalosome and urosome length and width
measurements were determined for copepods. Since hooks were often all that remained
of chaetognaths in the guts, a maximum hook length to body length regression for Pacific
Sagitta elegans (Terazaki 1993) was used to estimate body length, and a head width to
body length ratio for the same species (Pearre 1980) was used to estimate body width.
Total length and width were determined for all remaining prey for which body
measurements were possible. For well-digested prey, average body measurements from
intact, related taxa were used. Body measurements of prey items were used to calculate
body volume using formulae for the most similar geometric shape. Prey volume was
then used to determine wet weight (assuming specific gravity = 1.0 g cc-1). Crustacean
dry weight was calculated as 20% of wet weight and carbon as 40% of dry weight (Silver
and Gowing 1991, Steinberg et al. 1998). Conversion factors for other, less abundant
prey taxa were utilized as described in Larson (1986) and Steinberg et al. (1998).
General diet description
The diet of each myctophid species was summarized using three diet indices,
percent frequency of occurrence, percent composition by number, and percent dry weight
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after Hyslop (1980). The indices, represented below as %Ij, were calculated using a
cluster sampling estimator (Buckel et al. 1999, Latour et al. 2008) of the form:
100%
1
1
n
iik
ik
n
iik
j
M
qMI (1)
such that
j k
k
n
j
n
kijk
n
kijk
ik
w
wq
1 1
1 (2)
where n is the number of cod ends containing predator k, Mik is the number of predator k
collected in cod end i, nj is the number of prey types observed in stomachs of all predator
k, and nk is the number of predator k stomachs examined. In equation (2), qik represents
the proportion of occurrence, abundance, or weight of each prey type in each cod end.
Diet composition indices were calculated as a weighted average of qik with the abundance
of each predator, Mik, as the weighting factor. The variance for each diet index was
calculated as
21
22
2100
1
)(1
)var(%
n
IqM
MnI
n
ijikik
j (3)
after Latour et al. (2008), where M is the average number of predator k collected in a cod
end.
16
Ontogenetic and spatial changes in diet
The diets of many fishes change as they increase in size due to an increase in gape
allowing them to exploit bigger or different prey. To examine the effect of fish size on
the diet, individuals of each species were grouped into narrow size classes with the
members of each class having a relatively similar diet composition. Benthosema glaciale
and P. arcticum were grouped into 5 mm size classes and the proportion of dry weight of
each prey type was calculated for each size class. The narrow size classes were grouped
into broader categories with similar prey composition based on prey weight using cluster
analysis (Euclidean distance, average linkage method) and a scree plot was used to
determine the number of clusters.
Canonical correspondence analysis (CCA, ter Braak 1986) is a method which
extracts the major gradients in the data that can be accounted for by the measured
explanatory variables (McGarigal et al. 2000). For B. glaciale and P. arcticum, CCA was
used to investigate the relationship between diet, ridge section (RR, CGFZ, FSZ, AZ; see
Figure 1), depth zone (0-200, 200-750, 750-1500, 1500-2300, >2300 m), and time of day
(day, dusk, night, and dawn). Each element of the response matrix for the CCA was the
mean percent weight of a given prey type in a particular depth, ridge-section, and time-
of-day combination. In CCA, variability is explained by the canonical axes. The
canonical axes are linear combinations of the independent explanatory variables which
are correlated to the dependent variables, in this case weighted averages of prey.
Significance of the explanatory variables was determined using ANOVA, and a biplot
was constructed to explore the relationships between the explanatory variables and prey
weight. The CCA was performed using R version 2.12.0.
17
Gastric evacuation and daily consumption
Daily consumption was calculated using an evacuation rate model based on Elliott
and Persson (1978). Consumption (Cd) was calculated as
krd SEhC 24 (4)
where 24 is the number of hours in a day, E is the evacuation rate, and krS is the average
stomach content weight of predator k from ridge section r. Evacuation rates at ridge-
section specific temperatures were determined using a regression of compiled myctophid
gut evacuation rates and temperatures (E = 0.0942e0.0708t, where t represents temperature)
from Pakhomov et al. (1996). Due to the wide latitudinal distribution of the sampling
area, myctophids experienced different temperatures at their daytime depths (200-750 m,
depth zone 2) between ridge sections. Depth zone 2 is the depth at which myctophids in
this study are assumed to reside during the bulk of digestion. Consumption was
calculated separately for each ridge section due to evacuation rate dependence on
temperature.
Active carbon export by diel vertical migration
Active carbon export to below 200 m via respiration of CO2, excretion of
dissolved organic carbon (DOC), and egestion of particulate organic carbon (POC) in the
form of fecal pellets was determined only for the RR and AZ. Migrator biomass, defined
as the difference between night and day integrated myctophid biomass in the 0-200 m
depth interval, could not be determined at the CGFZ and FSZ due to the lack of sufficient
diel sampling at these ridge sections. CO2 flux was calculated using the following
equation from Dam et al. (1995)
18
hRBF 12 (5)
where F is the CO2 flux by migrant myctophids (mg C m-2 d-1), B is the biomass of
migrant myctophids integrated to 200 m (mg DW m-2), R is the weight-specific
respiration rate at temperatures experienced by myctophids at their day time residence
depths at the RR or AZ (6.6 or 11.8°C, respectively; calculated using a myctophid
oxygen consumption versus temperature regression reported in Donnelly and Torres
(1988), which was converted to CO2 respired using carbon and oxygen atomic ratios), and
12h is the assumed length of time myctophids spend at depth over a 24-h day. A
respiratory quotient of 0.8 was used in the calculation of R (Brett and Groves 1979).
DOC excretion information for fishes is lacking, so the relationship of CO2 respiration to
DOC excretion in zooplankton (DOC excretion = 31% CO2 respiration) reported by
Steinberg et al. (2000) was used to estimate DOC excretion in myctophids. POC egestion
at depth was calculated using the prey carbon conversions discussed above. It was
assumed that 100% of stomach and intestinal contents of fish caught at the surface would
be released below 200 m. The average amount of carbon per unit dry weight of fish
biomass was determined for B. glaciale and P. arcticum and multiplied by the integrated
migrator biomass at the RR or AZ and by 12 hours. Myctophid dry weight was
determined using a wet weight-standard length regression for each species (Fock and
Ehrich 2010) and a wet weight-dry weight ratio (DW/WW = 22.64%) based on an
average of compiled wet weight-dry weight ratios for many individual myctophid species
(Carmo pers. comm.).
19
RESULTS
General diet description
Benthosema glaciale
Fifty-nine different prey types were identified in 201 positive stomachs (75% of
all stomachs dissected) to an array of taxonomic levels depending on the extent of
digestion. Copepods constituted the bulk of the diet by weight (52%), were the most
frequently occurring prey category (93% of stomachs), and were the most abundant prey
(90% of all prey items by number). The copepod Calanus finmarchicus was the
predominant copepod in the diet of B. glaciale and made up over one quarter of the diet
by weight alone. Euphausiids were another major component of the diet, constituting
37% of the diet by weight and occurring in 21% of stomachs, but were consumed in low
abundance (2% of all prey items by number). Chaetognaths and ostracods constituted 6%
and 3% of the diet by weight, respectively, while the remaining prey categories–
amphipods, gelatinous prey, fishes, polychaetes, pteropods, digested crustaceans, and
unidentified prey, made up 1% or less of the diet by weight.
Protomyctophum arcticum
The diet of P. arcticum comprised 26 different prey types from 74 positive
stomachs (97% of all stomachs dissected) and was made up primarily of copepods (68%)
and euphausiids (25%) by weight. Nearly all P. arcticum stomachs contained copepods
(93% of stomachs) with the large copepod Paraeuchaeta norvegica making up the
highest proportion of copepod weight (15%). Ostracods occurred in 37% of stomachs but
constituted only 6% of the diet by weight and 12% by number. Digested crustaceans and
20
unidentified prey were the only other prey found in the diet of P. arcticum and made up
less than 1% of the diet by weight and number.
Hygophum hygomii
Eighteen different prey types from 28 positive stomachs (72% of all stomachs
dissected) were identified in the diet of H. hygomii. Euphausiids made up the highest
proportion of the diet by weight (53%) and occurred in 57% of stomachs; however, they
accounted for only 7% of all prey items by number. Ostracods were eaten frequently and
in high numbers, occurring in 80% of stomachs, making up 37% of the diet numerically,
and constituting one quarter of the diet by weight. Copepods, mainly Pleuromamma sp.,
Candacia sp., and euchaetid species, were the most frequently consumed prey category
(84% of stomachs), and made up half of the diet by number and 15% by weight. Fishes,
amphipods, pteropods, and unidentified prey each made up 5% or less by weight,
although amphipods were found in over half of stomachs.
Ontogenetic and spatial changes in diet
Benthosema glaciale
The size range of B. glaciale included in this study was 10.7-66.9 mm standard
length (Figure 2). Cluster analysis and a scree plot indicated three clusters of B. glaciale
based on diet composition and fish size separated into 5 mm size classes (Figures 3A and
B). The clusters of size classes did not parse out into discrete groups of sequential fish
sizes (i.e. small, medium, large). Instead, medium and large size classes (>20 mm) were
intermixed within two clusters while the smallest sizes (10-19.9 mm) clustered together.
21
The clusters closely reflect the proportion of euphausiid weight in the diet. Fish in cluster
A (Figure 3A) did not contain euphausiids, fish in cluster B possessed a high proportion
of euphausiid weight in the diet, and fish in cluster C contained a low proportion of
euphausiid weight in the diet. Due to the lack of evidence of an ontogenetic shift in the
diet of B. glaciale beyond the smallest size classes, fish size was not included in
subsequent analyses.
Canonical correspondence analysis (CCA) indicated B. glaciale dietary changes
in relation to ridge section (p = 0.005) and time of day (p = 0.025) were significant at α =
0.05 whereas depth (p = 0.25) was not significant (Figure 4). The three explanatory
variables included in the CCA, depth, ridge section, and time of day, accounted for 30%
of the variability in the diet, collectively. The first and second canonical axes accounted
for 34% and 29% of the explainable variation, respectively. Ridge section corresponded
more closely with the first canonical axis than the second, and accounted for a greater
proportion of the explainable variation. The remaining significant explanatory variable,
time of day, was more closely correlated to the second axis.
Prey items constituting the bulk of the diet of B. glaciale from the three northern
ridge sections were similar to each other but different from prey items in the diet of B.
glaciale from the AZ (Figure 5A). The diets of B. glaciale from the RR, CGFZ, and FSZ
were comprised mainly of euphausiids, 35%, 44%, and 65% by weight, respectively. The
copepod Calanus finmarchicus ranked second in the RR and CGFZ, constituting 31%
and 25% of the diet by weight, respectively, while P. norvegica made up 6% of the diet
by weight in the RR and 7% in the CGFZ. After euphausiids, ostracods and P. norvegica
constituted 11% and 6% of the diet by weight, respectively, in the FSZ. The diets of B.
22
glaciale from the AZ differed from those of the three northern ridge sections in that
ostracods made up 59% of the diet by weight. Pleuromamma copepods (7% by weight)
were the only other prey to make up greater than 5% of the diet by weight in B. glaciale
from the AZ. Polychaetes were only found in diets of myctophids from the RR, and fish
prey and pteropods were only identified in diets from the FSZ. Gelatinous prey was
found in the stomachs of fish from the RR, FSZ, and AZ.
The diet of B. glaciale collected during the day was comprised mainly of C.
finmarchicus and euphausiids, 31% and 29% by weight, respectively (Figure 5B).
Unidentified Calanidae copepods were the primary prey (42% by weight) in the night
time diets, while chaetognaths (67%) were the predominant prey at dawn. Calanus
finmarchicus, pteropods, and fish prey were only identified in fishes collected during the
day and polychaetes were only found in dawn samples. It is unlikely that B. glaciale did
not consume C. finmarchicus during the night, rather that poor taxonomic resolution
prohibited identification to genus or species level.
Protomyctophum arcticum
The size distribution of P. arcticum was 18-44.5 mm standard length (Figure 2).
The cluster analysis and scree plot (data not shown) indicated there was no ontogenetic
change in the diet and, therefore, fish length was not included in the CCA. CCA
indicated depth (p = 0.03) to be the only significant factor at α = 0.05 whereas ridge
section (p = 0.46) and time of day (p = 0.23) were not significant. The three explanatory
variables included in the CCA, depth, ridge section, and time of day, accounted for 38%
of the variability in the diet, collectively (Figure 6). The first and second canonical axes
23
accounted for 38% and 32% of the explainable variation, respectively. Depth zone
corresponded more closely with the second canonical axis.
The main difference in P. arcticum diet with respect to depth was the high
proportion of euphausiids (31%) in fish collected from depth zone 2 (200-750 m) and the
absence of euphausiids in fish from depth zone 1 (0-200 m; Figure 7). Paraeuchaeta
norvegica was identified in greater proportion in depth zone 2 (18%) than depth zone 1
(7%). The main components in the diets of fish from depth zone 1 were the copepod
Metridia sp. (17%), ostracods (16%), C. finmarchicus (13%), and copepods of the family
Aetideidae (12%).
Hygophum hygomii
The size distribution of H. hygomii was 27.7-56 mm standard length. There were
too few H. hygomii at the smallest and largest sizes to allow for cluster analysis of this
species. Additionally, since H. hygomii was only caught at the AZ and only during the
day, CCA was not performed for this species.
Species interaction and the effect on spatial changes in diet
To investigate the effect of co-occurrence of B. glaciale and P. arcticum on the
feeding ecology of these two species, CCA was performed for two scenarios in which
fish species was added as an explanatory variable. In one scenario only cod ends in
which both B. glaciale and P. arcticum were caught were included, and in another
scenario all cod ends that caught at least one of the two species were included. When all
cod ends that caught at least one of the two species were included in the CCA (Figure
24
8A), ridge section and fish species were significant (p = 0.005 and p = 0.01, respectively)
at α = 0.05, while depth zone and time of day were not (p = 0.79 and p = 0.12,
respectively). The four explanatory variables included in the CCA, depth, ridge section,
time of day, and fish species, accounted for 25% of the variability in the diet,
collectively. The first canonical axis accounted for 28% of the explainable variation
while the second axis accounted for 23%. Ridge section corresponded more closely with
the first canonical axis and accounted for a greater proportion of the explainable
variation, while fish species corresponded more closely to the second axis. Due to the
difference in distribution of these two species, it was not surprising that ridge section and
fish species were significant.
When only cod ends that contained both species were included in the CCA
(Figure 8B), fish species was significant (p = 0.05) at α = 0.05 and time of day
approached significance (p = 0.08) which indicated that these two species, when caught
together, had significantly different diet compositions, and diets of both species differed
slightly between day, night, and dawn. The four explanatory variables accounted for
34% of the variability in the diet with the first canonical axis accounting for 33% of the
explainable variation and the second axis accounting for 24%. Fish species corresponded
more closely to the first canonical axis and time of day corresponded more closely with
the second axis.
Gastric evacuation and daily consumption
Gastric evacuation rates were calculated for each myctophid species using
average water temperatures experienced in the 200-750 m depth zone in each ridge
25
section. From the northernmost ridge section to the southernmost, average water
temperatures were 6.6 °C (RR), 4.9 °C (CGFZ), 7.6 °C (FSZ), and 11.8 °C (AZ), with the
decline in temperature at the CGFZ due to the unique physical characteristics of the
Subpolar Front, present in this area (Søiland et al. 2008). Evacuation rates increased with
increasing temperature and ranged from 0.13-0.22 h-1 (Table 2). The average total weight
of prey in the stomachs of B. glaciale was highest at the RR (3.6 μg DW prey fish-1) and
for P. arcticum at the CGFZ (0.09 μg DW prey fish-1). Average total weight of prey was
lowest for B. glaciale in the AZ (0.02 μg DW prey fish-1) and for P. arcticum in the RR
(0.03 μg DW prey fish-1). Hygophum hygomii was only caught at the AZ and the average
total weight of prey in the stomachs was 0.92 μg DW prey fish-1. Daily consumption
rates per fish were calculated for each species at each ridge section (Table 2), converted
to consumption per unit of average myctophid biomass at each ridge section, and were
multiplied by the biomass of all myctophid species combined integrated to 2300 m to
provide a range of possible daily consumption estimates of MAR myctophids. Estimated
daily consumption of prey inferred for all MAR myctophids ranged from 0.34-42.02 μg
DW m-2 d-1 at the RR, 1.54-28.37 μg DW m-2 d-1 at the CGFZ, 6.83 μg DW m-2 d-1 at the
FSZ, and 0.72-3.35 μg DW m-2 d-1 at the AZ. Daily consumption in proportion to
myctophid body weight was always less than 1% for each species regardless of ridge
section.
Active carbon export by diel vertical migration
Active transport of carbon by diel vertically migrating myctophids was calculated
for ridge sections at which both day and night tows were performed in depth zone 1 (0-
26
200 m) and for which night time myctophid biomass was greater than day time
myctophid biomass in depth zone 1. The RR and AZ were the only ridge sections that
met these criteria. Respiration of CO2 by the 0-200 m integrated migrant myctophid
biomass was 0.01 mg C m-2 d-1 at the RR and 0.27 mg C m-2 d-1at the AZ (Table 3).
Myctophid excretion of DOC (calculated as 31% of myctophid respiration-see Methods)
was 0.003 mg C m-2 d-1 at the RR and 0.08 mg C m-2 d-1 at the AZ. Egestion of POC was
determined for B. glaciale at the RR and AZ and for P. arcticum at the RR. Hygophum
hygomii was only collected during the day and therefore migrant biomass and carbon
export could not be calculated for this species. Egestion rate of POC by B. glaciale
multiplied by the 0-200 m integrated migrant myctophid biomass resulted in export of
1.61 x 10-6 mg C m-2 d-1 at the RR and 1.71 x 10-4 mg C m-2 d-1 at the AZ. Substituting
egestion rate of POC by P. arcticum resulted in export of 7.08 x 10-6 mg C m-2 d-1 in the
RR. Total carbon transport by the migrant myctophid biomass in the RR and AZ was
estimated as 0.014 and 0.353 mg C m-2 d-1, respectively.
27
DISCUSSION
General diet description
Benthosema glaciale, P. arcticum, and H. hygomii were primarily
zooplanktivorous; however, the zooplankton composition and weight, frequency, and
abundance of prey varied among species. The overall diet composition of myctophids
from the ridge agrees with previous diet studies of these species (discussed below);
however, direct comparison to other studies of prey proportion in diets is not possible due
to the difference in sampling estimator used in this study (Equations 1 and 2). When
calculating diet indices of fish caught in active sampling gears it is important to consider
the sampling design used to collect the fish, as well as the species’ ecological
characteristics. Fish are known to aggregate in response to environmental gradients,
resource availability, and social behavior (Pitcher and Parrish 1993, Pakhomov and
Yamamura 2010); therefore, active sampling gear (such as the macrozooplankton and
Åkra trawls used in this study) are likely to collect groups of fish that are found together
in space and time based on a commonality, such as food availability. These groups are
likely to consume similar types of prey and in similar quantities and, thus, their diets are
likely to be more comparable to each other than to groups collected at different times or
locations (Latour pers. comm.). Therefore, in order to characterize the predatory impacts
of these fishes at the population level, these groups of fishes, rather than the individual,
should be considered the independent sampling unit (Bogstad et al. 1995, Buckel et al.
1999).
The simple random sampling (SRS) estimator is the predominant method used to
calculate diet indices of pelagic fishes (Hopkins and Gartner 1992, Moku et al. 2000) and
28
assumes that fishes are evenly distributed in the environment and have an equal
probability of capture (Cochran 1977). As discussed above, this assumption is often not
the case and, hence, the SRS estimator is not an appropriate method to use for calculating
diet indices of fishes with aforementioned ecological characteristics. In addition to
considering the ecology of the species, the appropriate sampling estimator can be
determined mathematically using the intracluster correlation coefficient (ICC, ρ) which
measures the relationship of the variance between groups of fish caught in different cod
ends to the variance within a group of fish caught in a single cod end. The parameter ρ
can be estimated for each prey type as
22
2
ˆˆ
ˆˆ
wb
b
ss
s
(6)
where 2ˆbs is the estimate of variance between groups and 2ˆws is the estimate of variance
within groups (Steel et al. 1997). As 2ˆws decreases towards 0 (signifying stomach
contents within cod ends are increasingly similar) ρ approaches 1. The ICC for several of
the most common prey types in the diet for each species ranged from 0.48-0.74 for B.
glaciale, 0.42-0.73 for P. arcticum, 0.84-0.98 for H. hygomii, indicating the diets of each
species within cod ends tend to be more similar than between cod ends. As a result, a
cluster sampling estimator, which treats the groups of fish in each cod end as the
independent sampling unit, was used to calculate dietary indices of these three species
from the MAR.
Of the three myctophid species included in this study, more is known about the
feeding ecology of B. glaciale than P. arcticum or H. hygomii. The diet of B. glaciale
from the MAR observed in this study was comprised predominantly of copepods by
29
weight, frequency of occurrence, and abundance. Calanus finmarchicus and euphausiids
made up the bulk of the diet by weight, with many other copepod taxa, amphipods,
ostracods, chaetognaths, pteropods, polychaets, fish, and unidentified gelatinous
zooplankton being consumed as well. Although not commonly identified in the diet,
myctophids do consume gelatinous prey. Several studies from the Gulf of Mexico
reported some larval and adult myctophid species fed on gelatinous prey, with some
larvae feeding almost exclusively on gelatinous zooplankton (Hopkins and Gartner 1992,
Conley and Hopkins 2004). Hopkins and Gartner (1992) reported gelatinous prey in the
diet of Benthosema suborbitale; however, to my knowledge, gelatinous prey has not been
reported in the diet of B. glaciale. Gelatinous prey was identified in the stomachs of
seven B. glaciale >40 mm from the MAR, equating to less than 1% of the numerical
abundance of prey in the diet. Due to the rapid digestion of gelatinous material, this
estimate represents an underestimate of gelatinous zooplankton in the diet of this species.
The diet of B. glaciale from the MAR agreed well with many previous studies of this
species which reported copepods, predominantly C. finmarchicus, Pleuromamma spp.
Metridia spp., and Paraeuchaeta norvegica, to comprise the bulk of the diet while the
fish also consumed euphausiids, ostracods, amphipods, pteropods, chaetognaths, and
fishes (Gjøsæter 1973, Kinzer 1977, Kawaguchi and Mauchline 1982, Roe and Badcock
1984, Petursdottir et al. 2008).
The diet of P. arcticum from the MAR was comprised mainly of copepods, with
P. norvegica constituting the bulk of the copepod component. Euphausiids and ostracods
were the only other identifiable prey in the diet. In a study from the Rockall Trough in
the North Atlantic, the diet of P. arcticum was also comprised mainly of copepods,
30
specifically Pleuromamma spp., as well as other copepods, such as Metridia sp. and
Aetideus sp., ostracods, and amphipods (Kawaguchi and Mauchline 1982). In the Davis
Strait west of Greenland, C. finmarchicus was the only identifiable prey of P. arcticum
(Sameoto 1989). The diet of H. hygomii from the MAR, mainly euphausiids and
copepods, also agreed well with previous studies; however, fish prey was surprisingly
abundant, constituting 5% of the diet by abundance at the MAR. In previous studies at
Great Meteor Seamount and in the Gulf of Mexico, H. hygomii fed on copepods,
amphipods, chaetognaths, euphausiids, mysids, ostracods, pteropods and unidentified
gelatinous prey (Hopkins and Gartner 1992, Pusch et al. 2004).
Diets of these three species likely reflect their different geographic distributions.
Benthosema glaciale occurred at all four ridge sections but was considerably less
abundant at the AZ, P. arcticum occurred at the three northern ridge sections, primarily
the RR and CGFZ, and H. hygomii was collected only from the AZ. Sutton et al. (2008)
identified a shift in the midwater fish assemblage composition from the three northern
ridge sections to the AZ, and a similar pattern was also observed in the distribution of
some copepod taxa. Gaard et al. (2008) found that the Sub-Polar Front (SPF) appeared to
act as a boundary to the horizontal distribution of several copepod species. Most
copepod genera that dominated north of the front were also present to the south but the
species were often different. The front appeared to restrict the northward distribution of
southern copepod genera more so than the reverse, as 14 genera were restricted to the
south of the SPF whereas only 4 were restricted to the north (Gaard et al. 2008). Some of
these patterns in copepod distribution were evident in the diet of the MAR myctophids in
this study, and are discussed below.
31
Ontogenetic and spatial changes in diet
Once general diet characteristics are known, it is useful to investigate what impact
certain biotic and abiotic variables have on the diet. Fish size is one factor that can
influence the composition of the diet. As a fish grows, different prey sizes and taxa
become available for exploitation and noting the changes in the diet is important in
understanding the ontogenetic changes in the ecology of the species. To avoid bias
associated with assigning fish to broad size bins with breaks at which dietary changes are
expected to occur, and then comparing the diets among those specified size bins, B.
glaciale and P. arcticum were, instead, assigned to small, 5 mm size bins, ensuring fish
within those bins had a relatively similar diet, and cluster analysis was used to determine
at what sizes dietary changes occurred. Again, due to a difference in methodology direct
comparison of ontogenetic dietary changes cannot be made with other studies but general
diet trends with size can be compared.
Cluster analysis indicated there were no ontogenetic changes in the diet of B.
glaciale beyond the smallest size classes, although three clusters were resolved (Figures
3A and B). The formation of these clusters was driven mainly by the weight of
euphausiids in the diet of fish within the 5 mm size classes. Cluster A contained the
smallest B. glaciale size classes included in this study, 10-19.9 mm. These fish did not
consume euphausiids but fed heavily on Pleuromamma copepods, ostracods, amphipods
and unidentified calanoid copepods. Fish >20 mm consumed euphausiids and were
clustered into two groups, those with a moderate proportion (cluster C) and those with a
high proportion (cluster B) of euphausiids (by weight) in the diet. Kinzer (1977) found
only B. glaciale >30 mm consumed euphausiids and amphipods, whereas diets of 20-24.9
32
mm B. glaciale in this study comprised 30% of the euphausiids by weight consumed by
all size classes, and the smallest B. glaciale size class (10-14.9 mm) consumed the
greatest proportion of amphipods. Size classes between 30-54.9 mm consumed the
highest proportion of C. finmarchicus copepods, suggesting that as B. glaciale increases
in size and larger prey items can be consumed, they do not exclude small prey items from
the diet (Dalpadado and Gjøsæter 1988, Sameoto 1988). Conversely, Kawaguchi and
Mauchline (1982) found the largest B. glaciale (36.1-62.5 mm) to exclude the smallest
copepods and substitute large prey such as euphausiids and fish. Similar trends of
exclusion were identified in the diets of other myctophid species as well (Hopkins et al.
1996, Pakhomov et al. 1996).
Cluster analysis indicated there was no ontogenetic change in diet of P. arcticum
sampled from the MAR, and only one cluster was identified. The main difference in the
diet amongst the different size classes was the high proportion of euphausiids (77% by
weight) in the largest size class 40-44.9 mm. Euphausiids were present in all other size
classes except the smallest (20-24.9 mm) but in much smaller proportions. Larger P.
arcticum also ate more of the large copepod P. norvegica. Ostracods were eaten in fairly
even proportions across all size classes while smaller P. arcticum tended to feed more
heavily on Metridia spp., C. finmarchicus and other calanoid copepods. To my
knowledge, aside from larval Protopmyctophum thompsoni (Sassa and Kawaguchi 2005),
detailed data of Protomyctophum spp. diet by size was previously unknown.
Sufficient sample size to perform a cluster analysis was not available for H.
hygomii but a general comparison of the diets within several size classes follows. The
diet across the different size classes (25-29.9, 35-39.9, 40-44.9, 45-49.9, and 50-59.9
33
mm) was very similar with most prey types occurring in each size class. Each of the size
classes consumed primarily euphausiids with the proportion of euphausiid weight ranging
from 52-82% of all prey weight in the size class. All H. hygomii size classes also
contained ostracods and the copepods Pleuromamma spp., Oncaea spp., and Candacia
spp. Fish prey only occurred in the 45-49.9 mm size class and pteropods occurred only in
the 40-44.9 mm size class. Pusch et al. (2004) reported the numerical diet composition of
H. hygomii in 10 mm size classes from 20-70 mm standard length. Copepods were the
most abundant prey in the diet of all size classes except the largest, of which amphipods
were the most abundant. Ostracods, pteropods, and euphausiids were consumed in low
numbers in all size classes. Data from this study agreed with Pusch et al. (2004) in that
copepods were eaten in high numbers in each size class; however, ostracods were eaten
in equal or greater amounts compared to copepods at small and large sizes and
amphipods were eaten in low abundance.
In addition to fish size, spatial and temporal factors also influence diet
composition. Several different water masses are present along the MAR within the study
site (Søiland et al. 2008). Water masses have different sources and characteristics such as
water temperature which can influence the distribution of zooplankton and fishes both
latitudinally and vertically and which, in turn, influences the available prey. Most
myctophids and zooplankton are diel vertical migrators to varying degrees, remaining in
isolumes throughout the water column that minimize the risk of predation but maximize
the opportunity for feeding (Pearre 2003, Cohen and Forward 2009, Ringelberg 2010,
Staby and Aksnes 2011). Some plankton undergo extensive migrations of hundreds of
meters, while others may only travel short distances (Angel 1989, Anderson and Sardou
34
1992). Depending on the depth and time of day at which myctophids feed, each species
could be feeding on a different prey field which would result in unique dietary
composition. Thus, time of day, depth, and latitude (represented by ridge section) were
included in a CCA to investigate the influence of these explanatory variables on the
variability in the diet.
The CCA indicated a significant change in the diet of B. glaciale with respect to
ridge section and time of day. As previously mentioned, the zooplankton community
composition south of the SPF differed from ridge sections north of the front for many
species and the shift in B. glaciale diet in the AZ reflects this change (Figure 5A). The
abundance of C. finmarchicus, the numerically dominant calanoid copepod north of the
SPF, declined by two orders of magnitude to the south of the front. This decrease in C.
finmarchicus abundance is reflected in the diet of B. glaciale as it was not identified in
the diet south of the SPF. The dominant components of B. glaciale diet in the three
northern ridge sections, C. finmarchicus and euphausiids, were replaced by ostracods in
the AZ. The separation of the AZ and corresponding prey from the other ridge sections
in the CCA biplot reflect these trends (Figure 4).
There were several interesting differences between the diets of B. glaciale caught
during the day, night, and dawn (there was only one dusk sample and, thus, it was not
included). The most surprising difference was the absence of C. finmarchicus from night
and dawn samples while constituting 31% of the diet by weight of B. glaciale during the
day. The absence of C. finmarchicus from the diet at night and dawn could be due to
mismatch in vertical distribution of predator and prey; although, Gaard et al. (2008)
reported C. finmarchicus was present from 0-2500 m at the MAR during the same
35
sampling period. Alternatively, the absence of C. finmarchicus could be an artifact of
poor taxonomic resolution and conservative identification as unidentified Calanidae
copepods made up 42% of night diets by weight. Chaetognaths made up a much greater
proportion of the diet by weight of B. glaciale during dawn, constituting 67% of the diet
by weight, versus 4% in day samples and <1% in night samples. However, the high
proportion of chaetognath weight in dawn samples could be anomalous as there were
only two (large) chaetognaths identified in these stomachs with the remaining prey
consisting of small copepods and ostracods. Other differences in diet with regard to time
of day include the presence of pteropods and fish only in day samples and polychaetes
only in dawn samples, although these items made up a very small proportion of the
weight and occurred in low abundance. The proportion of weight of most remaining prey
items were fairly consistent in day and night samples, while less than half of prey types
were identified in dawn samples.
Of the explanatory variables included in the P. arcticum CCA, the only significant
variable was depth. Protomyctophum arcticum was collected primarily from depth zones
1 and 2 and these were the only depths included in the CCA. Vertical migration can
influence the variety and quantity of prey available, however, vertical distribution and
diel vertical migration data for adult P. arcticum are lacking, making it difficult to
interpret how depth affects the diets of fish from different depths zones. Nafpaktitis
(1977) and Hulley (1984) report depths of P. arcticum maximum abundance during the
day and night in the North Atlantic to be 350 m (range of 250-850 m) and 250 m (range
of 90-325 m), respectively, suggesting P. arcticum may exhibit a weak vertical migration.
During the day, P. arcticum from the MAR exhibited typical patterns of abundance
36
corresponding to diel vertical migration, with abundance in depth zone 2 much higher
than in depth zone 1; however, night time abundance was nearly equal in depth zones 1
and 2 which could be due to a sizeable proportion of P. arcticum abundance remaining at
depth and not performing diel vertical migration (Watanabe et al. 1999). Alternatively,
the limited night time sampling at the two northern ridge sections may not have been
adequate to capture the true migratory pattern of this species, as the typical pattern of
higher abundance at depth in the day, and surface waters at night, of P. arcticum was
recorded during a subsequent MAR-ECO expedition to the CGFZ in 2009 (Cook et al. in
press).
The main difference in P. arcticum diet between depth zones 1 and 2 was the
presence of euphausiids only in stomachs collected during the day in depth zone 2,
constituting 31% by weight of the diets from this depth. The observed difference in
euphausiids with depth may be due to euphausiid diel vertical migration. However,
abundances of euphausiids were much higher in depth zone 2 than in depth zone 1 during
both day and night (unpublished data). It is unlikely that fish size is the underlying
factor dictating euphausiid consumption as there was only a 4 mm increase in average P.
arcticum size from depth zone 1 (28.4 mm SL) to depth zone 2 (32.1 mm SL) and the
size range of P. arcticum that consumed euphausiids encompassed the average length of
fish in each depth zone (28-44.5 mm SL). Other characteristics of P. arcticum diet from
depth zones 1 and 2 include aetideid copepods, C. finmarchicus, Metridia sp., and
ostracods, all of which are known vertical migrators (Al-Mutairi and Landry 2001,
Irigoien et al. 2004), constituting a considerably greater proportion of the diet by weight
37
in depth zone 1, while P. norvegica made up a greater proportion in depth zone 2. Other
prey were generally consumed in similar proportions at both depths.
In an attempt to determine if co-occurring species consume similar prey, CCA
was performed including diet data of both B. glaciale and P. arcticum. Both species
exhibited different horizontal distributions along the MAR and, consequently, were
exposed to different prey fields, especially B. glaciale south of the SPF. To remove the
influence of contrasting distributions, only B. glaciale and P. arcticum that were caught
together in the same cod end were included. Fish species was a significant explanatory
variable which indicates the diets of these two species, when caught together, are
significantly different. In many cod ends where both species were caught, prey items
identified in the stomachs of one species were typically absent or consumed in much
lower proportion by the other species (Table 4). Time of day also approached
significance when only co-occurring samples were included, driven mainly by rare prey
and prey types that made up a high proportion of the weight which were eaten at only one
time of day. Although niche overlap is not calculated here due to a lack of consensus as
to which measure is most accurate and least biased (Smith and Zaret 1982), these
differences in diet may suggest that some degree of resource partitioning could exist to
reduce competition. It must be kept in mind, as always, that the differences in the diet
could partially be due to poor taxonomic resolution.
Daily Consumption
The maximum daily consumption as a percentage of dry body weight for
myctophids in this study was 0.01%, below minimum values from previous studies.
38
Although a variety of methods have been used and direct comparisons are not possible,
the consensus is that myctophids generally consume <1-6% of dry body weight per day,
with most estimates closer to 1% (see table 6.2 in Brodeur and Yamamura (2005) and
sources therein). Average water temperature in depth zone 2 was lowest at the CGFZ and
highest at the AZ and, thus, calculated evacuation rates followed the same pattern since
evacuation rate is typically positively correlated with temperature to a maximum (Table
2) (Elliott and Persson 1978 and sources therein). Daily consumption by B. glaciale was
highest at the RR and decreased to the AZ, while daily consumption by P. arcticum
increased from the RR to the CGFZ. Hygophum hygomii was only collected in the AZ
and consumed a moderate amount compared to B. glaciale. Daily consumption estimates
for MAR myctophids presented here are likely to be an underestimate as a result of the
sampling design employed on the G.O. Sars cruise. Shallow depth zones were sampled
first and, thus, myctophids collected in depth zones 1 and 2 would continue digesting for
many hours after capture while the deeper depths were sampled. This prolonged
digestion would result in an underestimation of prey abundance in stomachs and,
consequently, underestimation of prey weight as a percentage of fish body weight.
Additionally, estimation of daily consumption of diel vertically migrating subarctic
myctophid species, which assumes only surface feeding at night, can be underestimated
due to active feeding during the day at depth. If day time feeding is not accounted for, it
could lead to an underestimate of the true daily consumption (Brodeur and Yamamura
2005). Although day time feeding was observed in both B. glaciale and P. arcticum, the
number of feeding periods over a 24 hour cycle could not be discerned from stomach
fullness data.
39
In order to accurately estimate the amount of prey consumed by the MAR
myctophid assemblage, an accurate estimate of myctophid biomass is required.
Midwater trawls have been the predominant tool used to estimate fish biomass in the past
but acoustic measurements are becoming increasingly more common and are shedding
light on inaccuracies of midwater trawls. Kaartvedt et al. (2012) estimated the sampling
efficiency of a large (~400 m2 mouth area) Harstad trawl using acoustics to verify the
catch of B. glaciale. They found B. glaciale was capable of avoiding the large trawl to
such an extent that the sampling efficiency was 14%. A similarly low sampling
efficiency was determined by Koslow et al. (1997) for a medium-sized IYGPT trawl (105
m2 mouth area). In the present study, myctophid biomass was estimated using the small
(36 m2 mouth area) macrozooplankton trawl since the fixed mouth area of this trawl
allowed for a more accurate calculation of volume of water filtered than the large (~660
m2 mouth area) Åkra trawl. Heino et al. (2011) determined the Åkra trawl to be more
efficient at catching fish than the macrozooplankton trawl with a relative catchability of
2.3. Because B. glaciale appears to be capable of avoiding even large midwater trawls,
the sampling efficiency of the macrozooplanton trawl could potentially be even lower
than 14% for large, stronger swimming myctophids, while the smaller mesh of the
macrozooplankton trawl would retain small fish better than the Åkra trawl.
The daily consumption by the MAR myctophid biomass reported in Table 2 is
based on the myctophid biomass collected with the macrozooplankton trawl. If the 14%
efficiency estimation reported by Koslow et al. (1997) and Kaartvedt et al. (2012) is
applied here, the daily consumption of the MAR integrated myctophid biomass feeding in
the 0-200 m depth zone at night ranges from 0.1-18 ug DW m-2 d-1 in the RR, 14 ug DW
40
m-2 d-1 in the FSZ, and 4-18 ug DW m-2 d-1 in the AZ (myctophids were not caught at
night in depth zone 1 at the CGFZ). Zooplankton biomass was not estimated at the
MAR, so integrated zooplankton biomass estimates were used from Gallienne et al.
(2001) in the area of 47°N 20°W in the North Atlantic during July, 1996 for the RR
(reported carbon values converted to dry weight using the conversion carbon = 40%
DW), and 0-200 m integrated values from the Bermuda Atlantic Time-series Study
(BATS) station in the Sargasso Sea during June and July, 2004 (http://bats.bios.edu/,
Steinberg et al. 2012) for the AZ to estimate the portion of the zooplankton biomass
removed daily. Gallienne et al. (2001) reported zooplankton biomass in the North
Atlantic was 763.5 mg DW m-2 (vertically integrated to 200 m), and average nighttime
zooplankton biomass at the BATS station was 735 mg DW m-2. Applying the B. glaciale
consumption rate to the RR and the H. hygomii consumption rate to the AZ integrated
migrant myctophid biomass adjusted for gear efficiency resulted in the removal of <1%
of zooplankton biomass at each ridge section every night. Estimated removal rates at the
MAR were lower than daily zooplankton removal rates by myctophids reported in
previous studies: 1-4% of zooplankton standing stock in the upper 150 m in the western
North Pacific (Watanabe et al. 2002), 2% in the upper 200 m in the Gulf of Mexico
(Hopkins and Gartner 1992), and 5-20% in the upper 300 m in the Southern Ocean
(Pakhomov et al. 1999).
Active carbon export by diel vertical migration
Diel vertically migrating zooplankton contribute to the vertical export of carbon
from the euphotic zone through respiration, excretion, and egestion (Longhurst et al.
41
1990, Schnetzer and Steinberg 2002), which could be an important source of carbon for
non-migrating mesopelagic zooplankton, and for bacteria, which are ultimately reliant on
surface-derived production (Steinberg et al. 2008). Diel vertically migrating fishes also
have the potential to contribute to the active transport of carbon; however, only one study
has quantified the contribution of mesopelagic fishes to the active transport of carbon to
meso- and bathypelagic depths (Hidaka et al. 2001). Myctophids are the most abundant
vertically migrating mesopelagic fishes in many areas, including the MAR, thus it is
important to include active carbon transport for these mesopelagic fishes as potential
contributors to the biological pump.
These estimates of active carbon transport out of the euphotic zone can be
compared to passive POC flux measured by sediment traps to explore the relative
importance of active vs. passive transport as components of the biological pump
(Steinberg et al. 2000, Hidaka et al. 2001). Passive POC flux data from the MAR is
currently unavailable and, hence, direct comparison to myctophid carbon export cannot
be made for the MAR. There are, however, numerous measurements of sediment trap
POC flux in the North Atlantic, mainly during the time of the North Atlantic spring
bloom. Using results from several studies in the North Atlantic during April and May
(Bender et al. 1992, Buesseler et al. 1992, Ducklow et al. 1993, Harrison et al. 1993,
Martin et al. 1993), a range of passive POC flux values measured with sediment traps
were compiled to compare to active transport by vertically migrating MAR myctophids.
Sampling during the G.O. Sars cruise was performed during a post bloom period (Gaard
et al. 2008) and, therefore, POC sinking rates would be lower than those during the spring
bloom. The present study estimated the active transport of carbon out of the surface 200
42
m, but the compiled POC flux data were measured at 150 m and 300 m, so comparisons
are made with flux data at both depths.
The migrant myctophid biomass was 5.2 mg C m-2 (integrated to 200 m) in the
RR and 40 mg C m-2 in the AZ, and active transport of CO2, DOC, and POC during
summer by MAR myctophids was ≤1% of passively sinking POC in the North Atlantic at
150 m and 300 m (Table 3). Another study investigating active carbon export by
myctophids in the western equatorial North Pacific Ocean found myctophid biomass
(uncorrected for net sampling efficiency) was 249-462 mg C m-2 from 0-160 m, and
active transport through respiration and egestion was 1.2-2.2 mg C m-2 d-1, equivalent to
2.0-3.7% of passively sinking POC (Hidaka et al. 2001, stations 15 and 16). Hidaka et al.
(2001) adopted the 14% sampling efficiency estimated by Koslow et al. (1997) which
dramatically increased their migrating myctophid biomass estimate (1778-3303 mg C m-2)
and, subsequently, carbon export (8.4-15.4 mg C m-2 d-1, 14.3-26.4% of passively sinking
POC). If the same sampling efficiency is applied to MAR myctophid biomass, active
transport increases to 0.1 mg C m-2 d-1 in the RR and 2.5 mg C m-2 d-1 in the AZ,
equivalent to 0.1-1.0% of sinking POC at 150 m and 0.3-3.5% at 300 m. The very high
migrant myctophid biomass in the Pacific is the reason for the considerably higher active
carbon transport estimated there compared to the MAR. MAR myctophid active
transport is also lower than the long-term (1994-2011) annual average zooplankton active
transport in the subtropical North Atlantic measured at the BATS station. There,
zooplankton transported 4.1 mg C m-2 d-1 via respiration, excretion, and egestion at depth,
which was, on average, 15% of sinking POC flux (Steinberg et al. 2012).
43
Due to the rapid decline of sinking POC with increasing depth, the carbon
transported by vertically migrating myctophids–of which some species migrate to 1000 m
or more, becomes increasingly important at greater depths. As a rough comparison,
Honjo and Manganini (1993) report passive POC flux at 1000 m in the North Atlantic
during April of 4.1 mg C m-2 d-1. Using corrected MAR myctophid biomass, the
myctophid carbon export measured in this study would be equivalent to 61% of sinking
POC at 1000 m. A few factors would decrease the amount of carbon transported to this
depth, however. A smaller proportion of the migrating myctophid biomass resides at
1000 m during the day, and greater migration distance means increased time for digestion
to occur resulting in a smaller proportion of POC actively exported out of the euphotic
zone being released at 1000 m. Nevertheless, the high proportion of carbon exported by
myctophids in relation to POC flux at greater depths reaffirms the importance of
myctophids in the biological pump and sequestration of carbon in the deep sea, and
suggests that myctophid active transport should be considered in carbon cycling models.
44
CONCLUSION
Overall, the diet of the three species of myctophids from the MAR analyzed in the
present study agreed well with previous investigations of these species in off-ridge areas
of the North Atlantic Ocean. However, the most abundant myctophid, B. glaciale,
possessed some unique dietary and ecological characteristics not observed in this species
elsewhere, such as consumption of gelatinous prey, and consumption of euphausiids and
amphipods earlier in the fish’s life history (i.e., at smaller fish sizes), which may suggest
that the distinctive MAR ecosystem supports a unique food-web structure. It must be
kept in mind, however, that this study provides information for only a limited period of
time during the year and the conclusions cannot be extrapolated beyond the summer.
Additional sampling during different times of year is necessary to determine if the
differences observed in this study are characteristic of annual patterns at the MAR.
Despite the limited temporal scale of this study, the resulting myctophid feeding data
represents a necessary first step for the construction of a MAR food web for comparing
the trophic structure of the MAR to continental slope regions of the eastern and western
Atlantic.
Hidaka et al. (2001) provided an estimate of active carbon transport by
myctophids in the Pacific Ocean and the current study provides the first estimate for
Atlantic myctophids. Carbon transport by myctophids at the MAR during summer was
low compared to sinking POC flux measured in the upper mesopelagic zone during the
spring bloom, but may potentially account for a much greater proportion of exported
carbon at lower mesopelagic depths. Additional spatial and temporal sampling and
information on sampling efficiency of an array of trawl types are needed to develop more
45
robust estimates of active carbon transport by myctophids and other migrating fishes.
Despite the high abundance of myctophids throughout the world’s oceans, the present
study is only the second to quantify the active transport of carbon to mesopelagic depths
by these vertically migrating fishes. The inclusion of migrating fishes will lead to a more
comprehensive view of the biological pump, which has implications for fueling deep-sea
food webs, the microbial loop, and for sequestration of atmospheric CO2.
46
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54
Tab
le 1
. Pre
y co
mpo
siti
on f
rom
sto
mac
hs o
f B
enth
osem
a gl
acia
le, P
roto
myc
toph
um a
rcti
cum
, and
Hyg
ophu
m
hygo
mii
col
lect
ed d
urin
g a
crui
se to
the
Mid
-Atl
anti
c R
idge
dur
ing
June
-Jul
y, 2
004.
n is
the
sam
ple
size
, %W
is th
e
perc
ent d
ry w
eigh
t, %
N is
the
perc
ent c
ompo
siti
on b
y nu
mbe
r, a
nd %
F is
the
perc
ent f
requ
ency
of
occu
rren
ce o
f ea
ch
prey
taxa
. (-
) in
dica
tes
prey
was
abs
ent.
55
Pre
yn
%W
%N
%F
n%
W%
N%
Fn
%W
%N
%F
Cop
epod
a
Cal
anoi
daA
etid
eus
sp.
10.
360.
709.
464
0.66
1.38
2.99
--
--
Aet
ideu
s ar
mat
a-
--
-9
0.45
1.97
7.75
--
--
Aet
ideo
psis
sp.
10.
000.
000.
02-
--
--
--
-C
hiri
diel
la s
p.-
--
-1
0.29
0.43
1.71
--
--
Euc
hire
lla s
p.1
0.00
0.00
0.02
--
--
--
--
Gae
tanu
s sp
.1
0.01
0.01
0.34
21.
330.
612.
51-
--
-P
seud
ochi
rella
sp.
10.
000.
010.
34-
--
--
--
-A
etid
eida
e71
1.28
2.84
24.1
922
3.13
4.84
16.4
56
0.26
1.80
18.6
0C
alan
us s
p.16
49.
0016
.32
44.4
347
5.88
7.81
22.6
3-
--
-C
alan
us f
inm
arch
icus
388
27.8
851
.38
71.7
394
8.14
12.2
014
.78
--
--
Cal
anid
ae11
62.
884.
565.
8011
1.18
1.87
7.68
461.
337.
1654
.83
Can
daci
a sp
.-
--
-39
1.13
6.99
65.4
1C
anda
cia
arm
ata
10.
000.
000.
02-
--
--
--
-C
anda
ciid
ae5
0.04
0.06
0.07
--
--
--
--
Euc
haet
a sp
.1
0.00
0.00
0.02
--
--
--
--
Par
aeuc
haet
a sp
.1
0.01
0.00
0.01
--
--
10.
090.
122.
06P
arae
ucha
eta
norv
egic
a37
5.99
1.87
20.6
417
14.7
53.
8817
.72
60.
870.
708.
22P
arae
ucha
eta
tons
a1
0.00
0.00
0.02
--
--
10.
090.
122.
06E
ucha
etid
ae22
0.37
0.87
11.5
912
3.20
3.30
6.84
--
--
Het
eror
habd
us s
p.10
0.04
0.13
0.67
30.
240.
531.
62-
--
-H
eter
orha
bdus
com
pact
us1
0.00
0.00
0.02
--
--
--
--
Het
eros
tylit
es lo
ngic
orni
s1
0.00
0.00
0.02
--
--
--
--
Het
eros
tylit
es s
p.12
0.00
0.03
0.20
10.
260.
431.
50-
--
-
B. g
laci
ale
P. a
rcti
cum
H. h
ygom
ii
Tab
le 1
.
56
Tab
le 1
. con
tinu
ed
Pre
yn
%W
%N
%F
n%
W%
N%
Fn
%W
%N
%F
Het
eror
habd
idae
--
--
10.
010.
151.
54-
--
-M
etri
dia
sp.
870.
211.
254.
2171
6.27
12.2
022
.46
--
--
Met
ridi
a cu
rtic
auda
10.
000.
010.
13-
--
--
--
-M
etri
dia
luce
ns1
0.00
0.00
0.03
464.
797.
846.
45-
--
-P
leur
omam
ma
sp.
218
1.42
4.18
39.4
237
4.67
8.45
27.2
482
2.17
17.1
980
.24
Ple
urom
amm
a ab
dom
inal
is5
0.01
0.02
0.15
10.
110.
191.
0211
0.19
1.28
8.22
Ple
urom
amm
a bo
real
is5
0.01
0.02
0.08
--
--
--
--
Ple
urom
amm
a gr
acili
s2
0.00
0.00
0.04
--
--
--
--
Ple
urom
amm
a ro
bust
a1
0.00
0.00
0.02
--
--
--
--
Ple
urom
amm
a xi
phia
s1
0.00
0.00
0.02
--
--
--
--
Met
ridin
idae
480.
191.
033.
8720
3.06
4.54
17.3
8-
--
-P
arac
alan
us s
p.1
0.00
0.00
0.02
--
--
--
--
Spi
noca
lani
dae
10.
000.
000.
02-
--
--
--
-O
ther
Cal
anoi
da12
91.
263.
048.
8650
7.95
9.65
38.2
439
1.55
7.53
56.4
3C
yclo
poid
Onc
aea
sp.
210.
020.
779.
842
0.02
0.29
2.62
270.
065.
3655
.23
Poe
cilo
stom
atoi
da1
0.00
0.00
0.02
--
--
--
--
Sapp
hiri
na s
p.1
0.00
0.01
0.06
--
--
--
--
O
ther
Cop
epod
a20
0.52
0.98
12.4
210
1.39
2.11
10.4
54
0.15
1.02
14.8
2
Am
phip
oda
190.
340.
122.
21-
--
-17
4.92
5.12
51.5
9T
hem
isto
sp.
100.
090.
060.
40-
--
--
--
-T
hem
isto
com
pres
sa2
0.10
0.07
1.64
--
--
--
--
Phr
onim
a sp
.1
0.45
0.11
0.30
--
--
--
--
Hyp
eriid
ae14
0.21
0.28
1.37
--
--
10.
250.
271.
83
B. g
laci
ale
P. a
rcti
cum
H. h
ygom
ii
57
Tab
le 1
. con
tinu
ed
Pre
yn
%W
%N
%F
n%
W%
N%
Fn
%W
%N
%F
Eup
haus
iace
a34
28.6
81.
8217
.33
1424
.93
2.61
13.3
634
68.8
47.
4956
.56
Eup
haus
iidae
258.
350.
514.
08-
--
--
--
-
Myo
doco
poda
247
3.11
3.72
19.2
255
4.87
9.70
35.1
716
214
.45
37.1
280
.37
Con
choe
cia
sp.
20.
010.
010.
04-
--
--
--
-C
onch
oeci
a m
agna
20.
010.
010.
04-
--
--
--
-C
onch
oece
tta
acum
inat
a1
0.00
0.00
0.02
--
--
--
--
Con
choe
cilla
dap
hnoi
des
10.
000.
000.
02-
--
--
--
-C
onch
oeci
nae
60.
010.
010.
1013
1.52
2.30
4.26
--
--
Pte
ropo
da1
0.00
0.01
0.02
--
--
--
--
Lim
acin
a sp
.1
0.00
0.01
0.02
--
--
--
--
Cav
olin
iidae
--
--
--
--
20.
000.
232.
06
Gel
ata
60.
100.
371.
02-
--
--
--
-T
halia
cean
10.
010.
110.
30-
--
--
--
-
Cha
etog
nath
a13
6.08
1.05
5.48
--
--
--
--
Pol
ycha
eta
10.
010.
010.
05-
--
--
--
-O
stei
chth
yes
20.
080.
040.
00-
--
-1
3.49
0.20
5.40
Cru
stac
ea8
0.07
0.05
0.18
20.
510.
552.
14-
--
-U
nide
ntif
ied
prey
230.
791.
5611
.83
10.
400.
172.
052
0.14
0.31
7.46
B. g
laci
ale
P. a
rcti
cum
H. h
ygom
ii
58
Table 2. Evacuation rates and average daily consumption (μg DW d-1) per fish at each
ridge section (RR, Reykjanes Ridge; CGFZ, Charlie-Gibbs Fracture Zone; FSZ, Faraday
Seamount Zone; AZ, Azorean Zone) for Benthosema glaciale, Protomyctophum
arcticum, and Hygophum hygomii. Values in parentheses are potential daily consumption
(μg DW m-2 d-1) by the biomass of all myctophid species at each ridge section integrated
0-2300 m using the average consumption per unit fish biomass of each of the three
species. (-) indicates species was not collected from ridge section.
Ridge Section T°C
Evacuation
Rate (h-1) B. glaciale P. arcticum H. hygomiiRR 6.6 0.150 12.99 (42.02) 0.11 (0.34) -
CGFZ 4.9 0.133 6.99 (28.37) 0.28 (1.54) -FSZ 7.6 0.161 1.74 (6.83) - -AZ 11.8 0.217 0.10 (0.72) - 4.79 (3.35)
Daily Consumption
59
Table 3. Active transport of carbon (mg C m-2 d-1) by diel migrating myctophids from the
Reykjanes Ridge (RR) and Azorean Zone (AZ). Active transport of CO2 and dissolved
organic carbon (DOC) is for the 0-200 m integrated biomass of all myctophid species
combined. Active transport of particulate organic carbon (POC) is the average carbon
content of prey from night time 0-200 m Benthosema glaciale diets multiplied by the 0-
200 m integrated biomass of all myctophid species combined. Total myctophid carbon
export across 0-200 m is compared to average POC flux in the North Atlantic Ocean
from different locations and depths* during April and May.
* POC flux ranged from 86-259 mg C m-2 d-1 at 150 m and 37-72 mg C m-2 d-1 at 300 m (Bender et al. 1992, Buesseler et al. 1992, Ducklow et al. 1993, Harrison et al. 1993, Martin et al. 1993)
Ridge Section CO2 DOC POC Total
150 m 300 mRR 0.011 0.003 1.61x10-6 0.014 0.01-0.02 0.02-0.04
AZ 0.270 0.084 1.71x10-4 0.353 0.14-0.41 0.49-0.95
% of Average POC Flux*
60
Tab
le 4
. Pro
port
ion
of p
rey
wei
ght i
n ea
ch s
peci
es (
BG
, Ben
thos
ema
glac
iale
; PA
, Pro
tom
ycto
phum
arc
ticu
m)
in
each
cod
end
whe
re b
oth
spec
ies
wer
e ca
ught
sim
ulta
neou
sly.
Col
or s
cale
rep
rese
nts
rang
e of
val
ues,
wit
h w
arm
er
colo
rs d
enot
ing
high
er p
ropo
rtio
ns w
ithi
n ea
ch c
od e
nd.
Ridge Section
Cod end
Species
Aetideidae
Aetideus sp.
Calanidae
Calanus sp.
Calanus finmarchicus
Euchaetidae
Paraeuchaeta norvegica
Metridinidae
Metridia sp.
Metridia lucens
Pleuromamma sp.
Heterorhabdidae
Other Calanoida
Other Copepoda
Amphipoda
Hyperiidae
Euphausiacea
Euphausiidae
Myodocopoda
Crustacea
Gelata
Chaetognatha
Unidentified prey
BG
00
00
00
0.13
90.
037
00
0.01
20
0.04
00
0.24
60
00
0.09
90
0.03
10.
390
0.00
5
PA
00.
037
00
00
00.
325
0.36
00
0.08
90
0.18
90
00
00
00
00
0
BG
00
0.74
90.
251
00
00
00
00
00
00
00
00
00
0
PA
0.03
20.
010
00
00.
298
0.40
30
00.
016
0.03
00
0.14
60
00
00
00.
064
00
0
BG
0.01
40
0.28
70.
072
00
0.25
90
00
00
0.36
70
00
00
00
00
0
PA
00
00.
030
00.
081
00
0.01
30
00
00.
008
00
0.84
00
0.00
40.
024
00
0
BG
00
10
00
00
00
00
00
00
00
00
00
0
PA
00
00.
165
0.51
00
0.13
60
0.06
40
0.00
90
0.09
50.
020
00
00
00
00
0
BG
0.05
40
0.12
90.
226
00
0.23
20.
020
00
0.06
20
0.03
30
00
00
00
00
0.24
3
PA
00
0.02
80.
154
0.38
00
00.
055
0.23
90
00
0.12
80
00
00
0.01
70
00
0
BG
0.03
00
00.
035
00
00
0.01
70
00
0.18
10
00
00
00
00.
713
0.02
5
PA
00
0.06
90
00
0.61
80.
099
00
0.04
10
0.17
30
00
00
00
00
0
BG
00
0.05
30
0.00
90.
011
00
00
0.01
70
0.02
70
00
0.87
60
00
00
0.00
7
PA
0.00
80.
003
00.
131
0.06
50
00
0.06
00
00
0.01
30.
025
00
0.68
80
0.00
70
00
0
BG
0.00
60
0.01
10.
044
0.29
00.
009
0.15
40.
002
0.01
90
0.00
20
0.02
60
0.02
00.
217
0.11
20.
072
0.01
20
00
0.00
3
PA
0.10
10
00
00.
023
0.18
80
0.00
30.
006
0.00
30
0.00
90.
012
00
0.64
50
0.01
00
00
0
BG
0.00
70
0.00
60.
046
0.10
60
00.
002
0.00
40
0.00
20
0.00
30
00.
072
0.14
70.
605
00
00
0
PA
0.04
50
00.
015
00
0.10
90.
026
00.
453
0.00
70
0.09
10
00
0.19
20
0.02
40
00
0.03
9
BG
00
0.05
40.
009
00
00.
010
00
0.00
60
0.02
80
00
0.89
40
00
00
0
PA
0.15
70
00.
077
00
0.19
00
0.25
10
0.01
30.
029
0.05
80
00
00
0.22
60
00
0C
GF
Z10
78
RR
1037
CG
FZ
1044
CG
FZ
1077
RR
1029
RR
1030
RR
1032
RR
1002
RR
1023
RR
1028
61
Figure 1. Trawl sampling stations at four ridge sections along the northern Mid-Atlantic
Ridge from Iceland to the Azores during the 2004 R/V G.O. Sars MAR-ECO expedition.
62
Fig
ure
2. S
tand
ard
leng
th (
mm
) fr
eque
ncy
hist
ogra
ms
for
myc
toph
ids
incl
uded
in th
is s
tudy
. n
is th
e nu
mbe
r of
eac
h sp
ecie
s di
ssec
ted.
63
Figure 3. Cluster diagram (A) and scree plot (B) for Benthosema glaciale. The cluster
diagram represents the relationships among the diet compositions of 5 mm size classes of
B. glaciale. The scree plot was used to determine the number of clusters into which the
size classes of B. glaciale should be grouped.
64
A B C
A
B
65
Figure 4. Canonical correspondence analysis biplot for Benthosema glaciale. Bolded
labels represent the centroids for each level of the ridge section (Reykjanes Ridge, RR;
Charlie-Gibbs Fracture Zone, CGFZ; Faraday Seamount Zone, FSZ; Azorean Zone, AZ)
time of day, and depth zone (0-200 m, DZ 1; 200-750 m, DZ 2; 750-1500 m, DZ 3)
explanatory variables. Points represent prey types in the diet. The canonical axes
represent linear combinations of the explanatory variables. Ridge section and time of day
were significant at α = 0.05.
66
67
Figure 5. Diet composition (percent weight) of Benthosema glaciale presented by ridge
section (A) and time of day (B). Error bars represent standard error of the percent weight
values of each prey type in the diet of B. glaciale. n is the number of stomachs dissected
from each ridge section or time of day. Note differences in scale of y axis for ridge
sections and times of day.
68
Per
cent
Wei
ght
0
10
20
30
40
50
Per
cent
Wei
ght
0
10
20
30
40
50
Per
cent
Wei
ght
10
30
50
70
Prey
Aet
idei
dae
Cal
anid
ae
Cal
anus
sp.
C. f
inm
arch
icus
Euc
haet
idae
P. n
orve
gica
Met
ridi
nida
e
Met
ridi
a sp
.
Ple
urom
amm
a sp
.
Het
eror
habd
us s
p.
Het
eros
tylit
es s
p.
Can
daci
idae
Oth
er C
alan
oida
Onc
aea
sp.
Oth
er C
opep
oda
Am
phip
oda
Hyp
eriid
ae
Eup
haus
iace
a
Myo
doco
poda
Oth
er C
rust
acea
Pte
ropo
da
Gel
ata
Cha
etog
nath
a
Pol
ycha
eta
Ost
eich
thye
s
Uni
dent
ifie
d P
rey
Perc
ent W
eigh
t
10
30
50
70
Reykjanes Ridge
Charlie-Gibbs Fracture Zone
Faraday Seamount Zone
Azorean Zone
n = 84
n = 40
n = 66
n = 64
A
69
Perc
ent W
eigh
t
0
10
20
30
40
50P
erce
nt W
eigh
t
0
10
20
30
40
50
Prey
Aet
idei
dae
Cal
anid
aeC
alan
us s
p.C
. fin
mar
chic
usE
ucha
etid
aeP
. nor
vegi
caM
etri
dini
dae
Met
ridi
a sp
.P
leur
omam
ma
sp.
Het
eror
habd
us s
p.H
eter
osty
lites
sp.
Can
daci
idae
Oth
er C
alan
oida
Onc
aea
sp.
Oth
er C
opep
oda
Am
phip
oda
Hyp
erii
dae
Eup
haus
iace
aM
yodo
copo
daO
ther
Cru
stac
eaP
tero
poda
Gel
ata
Cha
etog
nath
aPo
lych
aeta
Ost
eich
thye
sU
nide
ntif
ied
Pre
y
Per
cent
Wei
ght
0
20
40
60
80
100
Day
Night
Dawn
n = 151
n = 68
n = 12
Figure 5. continued
B
70
Figure 6. Canonical correspondence analysis biplot for Protomyctophum arcticum.
Explanatory variables include ridge section, time of day, and depth zone. Depth zone
was significant at α = 0.05. For description of explanatory variables see Figure 4.
71
Figure 7. Diet composition (percent weight) of Protomyctophum arcticum, presented by
depth zone (Depth zone 1, 0-200 m; Depth zone 2, 200-750 m). Error bars represent
standard error of the percent weight values of each prey type in the diet of P. arcticum. n
is the number of stomachs dissected from each depth zone. Note differences in scale of y
axis for depth zones 1 and 2.
72
Figure 8. Canonical correspondence analysis biplot for Benthosema glaciale (BG) and
Protomyctophum arcticum (PA). A) includes all samples of each species. Ridge section
and fish species were significant at α = 0.05. B) includes only samples of each species
that were caught simultaneously. Fish species was significant at α = 0.05, time of day
approached significance (p = 0.08). Explanatory variables include fish species, ridge
section, time of day, and depth zone. For description of explanatory variables see Figure
4.
73
A
B
74
Vita Jeanna Marie Hudson
Born August 24, 1986 in Alexandria, VA. Graduated from Culpeper High School in 2004. Earned a B.S. in Biology and a minor in Chemistry from Christopher Newport University in 2008. Worked as a research assistant with graduate student Lance Gardner, Center for Coastal Resource Management, and Virginia Sea Grant at the Virginia Institute of Marine Science (VIMS). Entered the Master’s program in Fisheries Science at VIMS in 2009 under Dr. Tracey Sutton, and completed the program under co-advisors Drs. John Graves and Deborah Steinberg.